2. In this study, we investigated whether a broad range of herbivores feeding on the annual plant Brassica nigra affect interactions with flower visitors, whether the direction of interactions is predicted by the feeding modes (chewing and sap-feeding) and sites (above-and belowground) of the herbivores, and whether it results in fitness consequences for the plant. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Plant phenotypic plasticity in response to antagonists can affect other community members such as mutualists, conferring potential ecological costs associated with inducible plant defence. For flowering plants, induction of defences to deal with herbivores can lead to disruption of plant–pollinator interactions. Current knowledge on the full extent of herbivore‐induced changes in flower traits is limited, and we know little about specificity of induction of flower traits and specificity of effect on flower visitors. We exposed flowering Brassica nigra plants to six insect herbivore species and recorded changes in flower traits (flower abundance, morphology, colour, volatile emission, nectar quantity, and pollen quantity and size) and the behaviour of two pollinating insects. Our results show that herbivory can affect multiple flower traits and pollinator behaviour. Most plastic floral traits were flower morphology, colour, the composition of the volatile blend, and nectar production. Herbivore‐induced changes in flower traits resulted in positive, negative, or neutral effects on pollinator behaviour. Effects on flower traits and pollinator behaviour were herbivore species‐specific. Flowers show extensive plasticity in response to antagonist herbivores, with contrasting effects on mutualist pollinators. Antagonists can potentially act as agents of selection on flower traits and plant reproduction via plant‐mediated interactions with mutualists.
Plant phenotypic plasticity in response to herbivore attack includes changes in flower traits. Such herbivore-induced changes in flower traits have consequences for interactions with flower visitors. Here, we synthesize current knowledge on the specificity of herbivore-induced changes in flower traits, the underlying molecular mechanisms and the ecological consequences for flower-associated communities. Herbivore-induced changes in flower traits seem to be to a large extent herbivore-species-specific. The extensive plasticity observed in flowers influences a highly connected web of interactions within the flower-associated community. We argue that the adaptive value of herbivore-induced plant responses and flower plasticity can only be fully understood from a community perspective, rather than from pairwise interactions. Flowers and their environment The angiosperms, which comprise the majority of plant species, are characterized by an incredible diversity in flowers that range from the tiny millimetre-long flowers of duckweed (Lemna minor) to the giant meter-wide corpse flower (Rafflesia arnoldi) [1, 2]. The diversity of
1. Plants show ontogenetic variation in growth-defence strategies to maximize reproductive output within a community context. Most work on plant ontogenetic variation in growth-defence trade-offs has focussed on interactions with antagonistic insect herbivores. Plants respond to herbivore attack with phenotypic changes. Despite the knowledge that plant responses to herbivory affect plant mutualistic interactions with pollinators required for reproduction, indirect interactions between herbivores and pollinators have not been included in the evaluation of how ontogenetic growth-defence trajectories affect plant fitness. 2. In a common garden experiment with the annual Brassica nigra, we investigated whether exposure to various herbivore species on different plant ontogenetic stages (vegetative, bud or flowering stage) affects plant flowering traits, interactions with flower visitors and results in fitness consequences for the plant. 3. Effects of herbivory on flowering plant traits and interactions with flower visitors depended on plant ontogeny. Plant exposure in the vegetative stage to the caterpillar Pieris brassicae and aphid Brevicoryne brassicae led to reduced flowering time and flower production, and resulted in reduced pollinator attraction, pollen beetle colonization, total seed production and seed weight. When plants had buds, infestation by most herbivore species tested reduced flower production and pollen beetle colonization. Pollinator attraction was either increased or reduced. Plants infested in the flowering stage with P. brassicae or Lipaphis erysimi flowered longer, while infestation by any of the herbivore species tested increased the number of flower visits by pollinators. 4. Our results show that the outcome of herbivore-flower visitor interactions in B. nigra is specific for the combination of herbivore species and plant ontogenetic stage. Consequences of herbivory for flowering traits and reproductive output were strongest when plants were attacked early in life. Such differences in selection pressures imposed by herbivores to specific plant ontogenetic stages may drive the evolution of distinct ontogenetic trajectories in growth-defence-reproduction strategies and include indirect interactions between herbivores and flower visitors.This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Additional supporting information may be found online in theSupporting Information section. How to cite this article: Rusman Q, Lucas-Barbosa D, Hassan K, Poelman EH. Plant ontogeny determines strength and associated plant fitness consequences of plant-mediated interactions between herbivores and flower visitors. J Ecol.
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